Diversity of Feather Mites (Acari: Astigmata) on Darwin's Finches Author(s): Scott M. Villa , Céline Le Bohec , Jennifer A. H. Koop , Heather C. Proctor , and Dale H. Clayton Source: Journal of Parasitology, 99(5):756-762. 2013. Published By: American Society of Parasitologists DOI: http://dx.doi.org/10.1645/12-112.1 URL: http://www.bioone.org/doi/full/10.1645/12-112.1

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. J. Parasitol., 99(5), 2013, pp. 756–762 Ó American Society of Parasitologists 2013

DIVERSITY OF FEATHER MITES (ACARI: ASTIGMATA) ON DARWIN’S FINCHES

Scott M. Villa, Celine´ Le Bohec*, Jennifer A. H. Koop†, Heather C. Proctor‡, and Dale H. Clayton Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, Utah 84112. Correspondence should be sent to: [email protected]

ABSTRACT: Feather mites are a diverse group of ectosymbionts that occur on most species of birds. Although Darwin’s finches are a well-studied group of birds, relatively little is known about their feather mites. Nearly 200 birds across 9 finch species, and from 2 locations on Santa Cruz Island, Gala´ pagos, were dust-ruffled during the 2009 breeding season. We found 8 genera of feather mites; the most prevalent genus was Mesalgoides (53–55%), followed by Trouessartia (40–45%), Amerodectes and Proctophyllodes (26–33%), Xolalgoides (21–27%), Analges and Strelkoviacarus (0–6%), and Dermoglyphus (2–4%). There was no evidence for microclimatic effects (ambient temperature and relative humidity) on mite diversity. Host body mass was significantly correlated with mean feather mite abundance across 7 of 8 well-sampled species of finches. Certhidea olivacea, the smallest species, did not fit this pattern and had a disproportionately high number of mites for its body mass.

Feather mites (Acari: Astigmata: Analgoidea, Pterolichoidea) their microhabitats on blue tits (Parus caeruleus) in response to are the most diverse groups of arthropods found on birds (Gaud seasonal changes in temperature. and Atyeo, 1996; Janovy, 1997; Proctor, 2003; Clayton et al., Despite their small geographic extent, the Gala´ pagos Islands 2010), with about 2,500 described species representing more than have a highly variable climate. Annual rainfall can vary by an 30 families (Mironov and Proctor, 2011). Feather mites are order of magnitude, and seasonal differences in rainfall strongly obligatory associates of birds that live on or in the skin, inside the influence finch evolution (Grant and Grant, 2008). Large quills, or on the surface of feathers. Depending on the taxon, they climatic differences are often present between microhabitats feed on uropygial oil, skin flakes, fungus, bacteria, and, to a lesser on the same island. Santa Cruz Island, in particular, provides extent, on the feathers themselves. Feather mites are highly good examples of changes in climate and vegetation that occur specialized for life on their hosts (Dabert and Mironov, 1999) and with increasing elevation (Grant and Grant, 2008). For they occur on almost all species of birds, with the likely exception example, climate between lowland arid zones and highland of penguins (Mironov and Proctor, 2008). scalesia zones differ significantly in relative temperature and Darwin’s finches are a well-studied group of birds endemic to humidity (Grant and Grant, 2008). These contrasting climatic the Gala´ pagos Islands (Grant, 1986). They are a monophyletic zones harbor a diversity of Darwin’s finches, some of which are group with 14 recognized species belonging to 5 genera (Grant found in both microhabitats. The major goal of this paper was and Grant, 2008); however, very little is known about the to test whether variation in abiotic factors such as temperature feather mites that inhabit Darwin’s finches. Previous knowledge and humidity shape feather mite communities of Darwin’s of these mites comes from studies that concentrated on ground finches. finches (Geospiza spp.). Mironov and Perez (2002) conducted a Host body mass can also influence feather mite diversity. survey that documented 2 species of mites associated with 4 Larger-bodied hosts provide more resources and therefore species of ground finches. Surveys by Lindstrom¨ et al. (2004, support larger populations of ectosymbionts (Poulin and Rohde, 2009) and OConnor et al. (2005) found that small ground 1997; Poulin, 2007). For instance, Ro´ zsa (1997) examined wing- finches (Geospiza fuliginosa)harbor7speciesoffeathermites dwelling feather mites on 17 species of Portuguese passerines and from 6 genera, but they included only 6 of 14 species of found that mite abundance was positively correlated with host Darwin’s finches. One important factor often overlooked when examining body mass. Similarly, Clayton and Walther (2001) found that ectosymbiont diversity is the impact of the host’s abiotic feather louse abundance was positively correlated with host body environment (Malenke et al., 2011). In particular, bird-associated mass across 52 species of Peruvian birds. Previous studies arthropod diversity can be influenced by many climatic factors examining the effect of host body mass on feather mite abundance (Merino and Potti, 1996; Møller, 2010). Unlike endosymbionts, examined individuals within a single finch species (Lindstrom¨ et which inhabit more stable environments regulated by host al., 2009). The body mass of Darwin’s finches varies 4-fold among physiology, ectosymbionts, like feather mites, can be influenced species. The smallest of Darwin’s finches, the warbler finch by variation in ambient temperature and humidity (McClure, (Certhidea olivacea), weighs about 8 g. The largest of the finches, 1989; Davidson et al., 1994; Janovy, 1997; Moyer et al., 2002; the large ground finch (Geospiza magnirostris), weighs about 35 g Møller, 2010). For instance, Moyer et al. (2002), Bush et al. (Grant and Grant, 2008). (2009), and Malenke et al. (2011) found that ambient humidity We set out to test 2 hypotheses concerning the potential impact influences the community structure of feather lice on different of (1) climate and (2) host body size on aspects of feather mite groups of birds. Wiles et al. (2000) found that feather mites shift diversity among Darwin’s finches. The first hypothesis was that, within host species, feather mite prevalence and abundance are Received 16 October 2012; revised 4 May 2013; accepted 14 May 2013. higher in more humid environments. The second hypothesis was * LEA 647 ‘BioSensib’ CSM-CNRS, 8 quai Antoine 1er, MC 98000, that, across host species, feather mite abundance is correlated Principality of Monaco. with body size; larger-bodied finch species have more mites per † Ecology and Evolutionary Biology, University of Arizona, P.O. Box individual. To test our predications, we quantified components of 210088, Tucson, Arizona 85721. ‡ Department of Biological Sciences, University of Alberta, Edmonton, the diversity (prevalence and abundance) of feather mites infesting Alberta T6G 2E9, Canada. 9 species of Darwin’s finches from 2 different locations on Santa DOI: 10.1645/12-112.1 Cruz.

756 VILLA ET AL.—FEATHER MITES ON DARWIN’S FINCHES 757

MATERIALS AND METHODS Mite diversity was compared between host species and sites using rank Study sites and birds abundance plots and Kolmogorov–Smirnov 2-sample tests. This allowed us to compare patterns of mite communities with respect to both richness Our study was conducted between January and April 2009 on Santa and relative evenness of mite genera (Magurran, 2004). Rank abundance Cruz Island in the Gala´ pagos Archipelago, Ecuador. Nine species of patterns of mite communities are thought to be more sensitive measures Darwin’s finches from 4 genera were sampled for feather mites: G. than species richness alone, and are less influenced by sampling bias than magnirostris, G. fortis, G. scandens, G. fuliginosa, Platyspiza crassirostris, Camarhynchus psittacula, C. parvulus, Cactospiza pallidus, and Certhidea diversity indices (Tokeshi, 1993). Statistical analyses were conducted in olivacea. JMPt v.9.0. Birds were sampled at 2 locations: a highland site near Los Gemelos 0 00 0 00 (LG; 0837 50.95 S, 90823 26.54 W), and a lowland site at the Charles RESULTS Darwin Research Station (CDRS) on Academy Bay, Puerto Ayora 0 00 0 00 (0844 27.55 S, 90818 10.10 W). The LG field site, which is located at an Microclimatic differences between sites altitude of 450 m, is a patchwork of humid nondeciduous forest consisting mainly of Tree scalesia (Scalesia pedunculata). Environmental descriptors Mean monthly temperature across the year differed significant- (ambient temperature and humidity) of the highlands were collected by a weather station (Climate DataZone) near the town of Bellavista, which is ly between the 2 sites (Fig. 1A; Student’s t-test, t ¼ 2.28, P ¼ 0.03). somewhat lower in elevation than LG, but with a comparable Mean monthly temperature (6 SE) in the highlands (LG) was microclimate (Dudaniec et al., 2007). The coastal CDRS field site, which 23.32 6 0.48 C compared with 24.78 6 0.43 C in the lowlands is at sea level, is hotter and drier than the highlands. The CDRS field site is characterized by arid adapted plants, such as Opuntia cacti, Croton (CDRS). Mean monthly relative humidity (RH) across the year scouleri, and the trees Bursera graveolens, Pisonia floribunda, and Piscidia also differed significantly between the 2 sites (Fig. 1B; t ¼ 3.84, P carthagenensis. Environmental descriptors of the lowlands (same as above) , 0.001). Mean monthly RH in the highlands was 84.75 6 1.74% were collected by a weather station at CDRS (Climate DataZone). compared with 80.06 6 1.37% in the lowlands. Feather mite collection Identical methods for capturing birds and collecting feather mites were used at both field sites. Birds were captured with mist nets between 0600 and 1100 hr or 1600 and 1800 hr, and placed individually in single-use paper bags to avoid mixing parasites among birds. Feather mites were collected using the dust-ruffling method (Walther and Clayton, 1997; Clayton and Drown, 2001). Birds were held in 1 hand over a cafeteria tray lined with clean, white paper. Over the course of about 1 min, 1 hand was used to work ca. 1 tsp. of dusting powder into the plumage of the wings, tail, keel, vent, back, head, and neck. Care was taken to avoid getting dust in the bird’s nostrils or eyes. The dust was a pyrethin-based powder containing 0.1% pyrethrins and 1.0% piperonyl butoxide (Zodiac Flea and Tick Powdert). Birds were held for 2 min to allow the powder to take effect. The feather tracts were then ruffled for a combined total of 1 min. Each bird was banded with a metal band, which allowed us to avoid resampling birds for mites. Dust and mites from the paper were funneled into a labeled vial of 70% ethanol.

Feather mite processing Upon return to the United States, contents of the vials were transferred directly to white 110-mm filter paper using distilled water. Papers were then sprayed gently with 95% ethanol before being folded and stored in individual plastic Ziploct bags. For quantification and identification of mites, the filter papers were placed over a plastic grid (1.3 cm) and examined using a microscope under 3100 magnification. Observers (C.L.B. and J.A.H.K.) examined the grid systematically to quantify and identify feather mites. Early in the study a subset of mite samples (exemplars of all observed morphotaxa) were sent to H.C.P. for identification, and the resulting guide was used by C.L.B. and J.A.H.K. for identification of mites. Slide-mounted exemplars of adults within each of these genera were used to represent a single morphospecies; however, because some taxa may have been present only as juveniles, it is possible that more than 1 species per genus was actually present. Since we could not be sure that there were no other species represented among the juvenile stages, we conservatively refer to all taxa at the genus rather than the species level. Mites were subsequently removed from the paper and stored in vials of 95% ethanol.

Statistics Mean monthly temperature and relative humidity at the 2 field sites were both compared using Student’s t-tests. Mite prevalence was compared between host species and sites using Fisher’s exact tests. Mite abundance was first log transformed (log [n þ 1]) to achieve normality, and values were compared between sites using Student’s t-tests. The FIGURE 1. (A) Mean monthly temperature and (B) humidity at the abundance of mites among finch species was compared using a 1-way highlands (Los Gemelos: LG) and lowlands (Charles Darwin Research analysis of variance with Tukey post hoc tests and sequential Bonferroni Station: CDRS) in 2009. The main breeding season (January–April) for corrections. finches, i.e., when all birds were dust-ruffled, is highlighted in gray. 758 THE JOURNAL OF PARASITOLOGY, VOL. 99, NO. 5, OCTOBER 2013

TABLE I. Prevalence of feather mites (%) on Darwin’s finches (OLI [Certhidea olivacea], PAR [Camarhynchus parvulus], FUL [Geospiza fuliginosa], PSI [C. psittacula], SCA [G. scandens], FOR [G. fortis], PAL [Cactospiza pallidus], CRA [Platyspiza crassirostris], MAG [G. magnirostris]) according to the habitat (A. highlands [Los Gemelos, LG] vs. B. lowlands [Charles Darwin Research Station, CDRS]). Feather mites are organized by family (Dermo ¼ Dermoglyphidae; Psoro ¼ Psoroptoididae; Troues ¼ Trouessartiidae; Xolal ¼ Xolalgidae) and genus (Analg ¼ Analges; Strelk ¼ Strelkoviacarus; Derm ¼ Dermoglyphus; Amero ¼ Amerodectes; Procto ¼ Proctophyllodes; Unkn ¼ Unknown; Mesal ¼ Mesalgoides; Trou ¼ Trouessartia; Xola ¼ Xolalgoides). Unknown indicates early instar juvenile feather mites that could only be identified to family and were either Amerodectes or Proctophyllodes.

Analgidae Proctophyllodidae Dermo Psoro Troues Xolal Host (n) Analg Strelk Derm Amero Procto Unkn Mesal Trou Xola

A. Highlands (LG) PAL (11) 0.0 0.0 9.1* 36.4* 45.5* 0.0 72.7* 36.4* 0.0 PAR (21) 0.0 4.8* 0.0* 28.6* 33.3* 4.8* 38.1* 23.8* 38.1* PSI (4) 0.0 0.0 0.0 25.0* 50.0* 0.0 75.0* 50.0* 25.0* OLI (20) 30.0* 10.0* 0.0 70.0* 15.0* 25.0* 60.0* 75.0* 50.0* FOR (16) 0.0 6.3* 0.0 18.8 25.0* 0.0 50.0 31.3 18.8 FUL (26) 0.0 0.0 3.8 15.4 30.8 3.8 50.0 50.0 15.4 Overall (98) 6.1 4.1 2.0 32.7 29.6 7.1 53.1 44.9 26.5 B. Lowlands (CDRS) PAL (1) 0.0 0.0 0.0 100.0* 0.0 0.0 100.0* 0.0 0.0 PAR (8) 0.0 12.5* 0.0 0.0 0.0 0.0 0.0 0.0 0.0 FOR (23) 0.0 0.0 4.3* 30.4 43.5* 8.7 60.9 56.5 30.4 FUL (15) 0.0 0.0 0.0 13.3 40.0 6.7 60.0 53.3 46.7 MAG (10) 0.0 0.0 0.0 50.0 30.0 10.0 70.0* 70.0 30.0* SCA (21) 0.0 0.0 9.5* 23.8 19.0* 4.8 52.4 38.1 14.3 CRA (23) 0.0 0.0 4.3* 30.4* 43.5* 4.3* 60.9* 21.7* 8.7* Overall (101) 0.0 1.0 4.0 26.7 32.7 5.9 55.4 40.6 21.8

* Indicates new host record.

Host species captured at each site Dermoglyphus spend most of their life cycle inside quills, and their relative rarity in the dust-ruffling samples may be due to their At the highland site (LG) we sampled 98 individuals living in this protected microhabitat (Proctor, 2003). Strelkovia- representing 6 species of Darwin’s finches: G. fortis, G. fuliginosa, carus has the body shape typically associated with skin-dwelling Camarhynchus psittacula, C. parvulus, Cactospiza pallidus, and feather mites (Gaud and Atyeo, 1996; Dabert and Mironov, Certhidea olivacea. At the lowland site (CDRS) we sampled 101 1999). Very small numbers of other mite taxa were collected, but individuals representing 7 species of finches: G. magnirostris, G. were not included in our analyses; these mites included a blood- fortis, G. scandens, G. fuliginosa, Platyspiza crassirostris, Cama- feeding Pellonyssus sp. (Mesostigmata: Macronyssidae) and rhynchus parvulus, and Cactospiza pallidus. detritus-feeding nest mites from the families Acaridae and Description of mite taxa found on Darwin’s finches Winterschmidtiidae (Astigmata).

Eight genera of analgoid feather mites (Acari: Astigmata), Comparison of mite diversity between sites representing 6 families, were collected (Tables I, II). Five of the 8 observed morphospecies are described species already known From the highland finch species, we collected 8 genera of from Darwin’s finches: Amerodectes (previously Pterodectes) feather mites (Tables IA, IIA). Across all highland birds, 70.4% atyeoi (OConnor et al., 2005), Mesalgoides geospizae Mironov (69/98) of finches were infested with at least 1 feather mite. Mite and Perez, 2002, Proctophyllodes darwini OConnor et al., 2005, richness ranged between 0 and 5 genera per individual host; Trouessartia geospiza OConnor et al., 2005, and Xolalgoides overall mite abundance (mean 6 SE) was 44.0 6 10.3 mites per palmai Mironov and Perez, 2002. Adults of the Analges, individual host. Overall mite abundance is the average number of Strelkoviacarus, and Dermoglyphus specimens appear to belong mites per host individual regardless of mite genera or host species. to as-yet-undescribed species. Five mite taxa were relatively common (prevalence .25%; Table Representatives of 4 mite genera—Mesalgoides, Trouessartia, IA); Mesalgoides was the most prevalent feather mite genus, being Proctophyllodes,andAmerodectes—were found on all nine found on 53.1% (52/98) of sampled finches. sampled Darwin’s finch species. Although most feather mite From the lowland finches, we collected seven genera of mites genera infested multiple host species, members of 1 genus, (Tables IB, IIB). Across all lowland birds, 62.4% (63/101) of Analges, were found exclusively on Certhidea olivacea. finches were infested with at least 1 feather mite. Mite richness Because of the dust-ruffling method of collecting we were not ranged between 0 and 5 genera per individual host; overall mite able to record microhabitats of the mite taxa, but typically abundance was 33.0 6 6.1 mites per individual host. Four mite members of the Proctophyllodidae and Trouessartiidae inhabit taxa were relatively common (prevalence .25%; Table IB); the vanes of flight feathers. Analges, Mesalgoides, and Xolalgoides Mesalgoides was also the most prevalent feather mite genus, being are associated with the downy parts of feathers. Species of found on 55.4% (56/101) of sampled finches. VILLA ET AL.—FEATHER MITES ON DARWIN’S FINCHES 759

TABLE II. Abundance (mean 6 SE) of feather mites on Darwin’s finches (OLI [Certhidea olivacea], PAR [Camarhynchus parvulus], FUL [Geospiza fuliginosa], PSI [C. psittacula], SCA [G. scandens], FOR [G. fortis], PAL [Cactospiza pallidus], CRA [Platyspiza crassirostris], MAG [G. magnirostris]) according to the habitat (A. highlands [Los Gemelos, LG] vs. B. lowlands [Charles Darwin Research Station, CDRS]). Feather mites are organized by family (Dermo ¼ Dermoglyphidae; Psoro ¼ Psoroptoididae; Troues ¼ Trouessartiidae; Xolal ¼ Xolalgidae) and genus (Analg ¼ Analges; Strelk ¼ Strelkoviacarus; Derm ¼ Dermoglyphus; Amero ¼ Amerodectes; Procto ¼ Proctophyllodes; Unkn ¼ Unknown; Mesal ¼ Mesalgoides; Trou ¼ Trouessartia; Xola ¼ Xolalgoides). Unknown indicates early instar juvenile feather mites that could only be identified to family and were either Amerodectes or Proctophyllodes.

Analgidae Proctophyllodidae Dermo Psoro Troues Xolal Host (n) Analg Strelk Derm Amero Procto Unkn Mesal Trou Xola

A. Highlands (LG) PAL (11) 0.0 0.0 0.1 (0.1)* 44.1 (30.1)* 2.8 (1.2)* 0.0 11.9 (4.8)* 2.5 (1.6)* 0.0 PAR (21) 0.0 0.1 (0.1)* 0.0 0.4 (0.1)* 11.0 (6.2)* 0.1 (0.1)* 2.8 (1.3)* 0.8 (0.4)* 2.2 (1.1)* PSI (4) 0.0 0.0 0.0 6.8 (6.8)* 8.3 (7.0)* 0.0 82.3 (71.1)* 1.0 (0.7)* 1.8 (1.8)* OLI (20) 3.0 (1.4)* 0.5 (0.4)* 0.0 24.2 (12.1)* 0.3 (0.2)* 1.6 (0.8)* 5.9 (2.7)* 53.2 (21.6)* 10.5 (3.8)* FOR (16) 0.0 0.1 (0.1)* 0.0 0.6 (0.4) 5.1 (3.3)* 0.0 25.5 (15.3) 9.9 (6.4) 0.6 (0.4) FUL (26) 0.0 0.0 0.04 (0.04) 0.2 (0.1) 1.6 (0.8) 0.1 (0.1) 3.3 (1.1) 2.5 (1.0) 0.8 (0.5) Overall (98) 0.6 (0.3) 0.1 (0.1) 0.02 (0.01) 10.4 (4.3) 4.3 (1.5) 0.4 (0.2) 11.5 (4.0) 13.6 (4.9) 3.0 (0.9) B. Lowlands (CDRS) PAL (1) 0.0 0.0 0.0 17.0* 0.0 0.0 9.0* 0.0 0.0 PAR (8) 0.0 0.1 (0.1)* 0.0 0.0 0.0 0.0 0.0 0.0 0.0 FOR (23) 0.0 0.0 0.3 (0.3)* 3.5 (2.3) 16.2 (7.4)* 0.5 (0.4) 8.7 (2.4) 4.2 (1.6) 0.7 (0.3) FUL (15) 0.0 0.0 0.0 0.3 (0.2) 3.9 (2.6) 0.9 (0.9) 4.8 (2.2) 7.3 (5.9) 1.8 (0.8) MAG (10) 0.0 0.0 0.0 26.9 (15.3) 23.7 (23.3) 2.4 (2.4) 43.8 (15.5)* 9.3 (3.9) 1.4 (1.1)* SCA (21) 0.0 0.0 0.4 (0.3)* 0.7 (0.4) 1.7 (1.0)* 0.1 (0.1) 7.8 (3.7) 1.0 (0.3) 0.3 (0.2) CRA (23) 0.0 0.0 0.2 (0.2)* 17.4 (12.6)* 6.4 (2.6)* 0.4 (0.4)* 13.6 (6.4)* 1.3 (0.9)* 0.2 (0.1)* Overall (101) 0.0 0.01 (0.01) 0.2 (0.1) 7.8 (3.3) 8.4 (2.9) 0.6 (0.3) 11.9 (2.5) 3.4 (1.1) 0.7 (0.2)

* Indicates new host record.

To compare the prevalence, abundance, and diversity of mites 194; r ¼ 0.08, P ¼ 0.29). However, we found a highly significant on conspecific hosts at the highland (LG) and lowland (CDRS) correlation between mite abundance and host body mass (n ¼ 174; sites, we used host species for which at least 10 individuals were r ¼ 0.25, P ¼ 0.0009) when Certhidea olivacea was removed from sampled per site (Tables IA, B, IIA, B). Two species met this the analysis. Indeed, C. olivacea showed significantly more feather criterion: G. fortis and G. fuliginosa. We found no significant mites than Camarhynchus parvulus (P , 0.001), G. fuliginosa (P , difference in mite prevalence (Fisher’s exact P ¼ 0.80) or 0.001), and G. scandens (P ¼ 0.01) (Fig. 3). abundance (t ¼ 0.94, P ¼ 0.35) between sites for G. fortis or G. fuliginosa (Fisher’s exact P ¼ 1.00; t ¼ 1.10, P ¼ 0.28). We found DISCUSSION no significant difference in mite diversity between the 2 sites (Fig. 2A, B) for G. fortis (Kolmogorov–Smirnov two-sample, D ¼ 4.63, Our study is the most comprehensive survey of feather mites P . 0.10) or G. fuliginosa (D ¼ 0.60, P . 0.10). from Darwin’s finches to date. To our knowledge, this is the first We also compared feather mite prevalence, abundance, and time feather mites have been recorded from Platyspiza crassi- diversity between the overall highland and lowland finch rostris, Camarhynchus psittacula, C. parvulus, Cactospiza pallidus, assemblages (Tables IA, B, IIA, B). There were no significant or Certhidea olivacea. From our 9 study species of finches, we differences between the 2 sites in overall prevalence (Fisher’s exact identified a total of 8 genera of feather mites, representing 6 mite P ¼ 0.65) or abundance (t-test, t ¼ 0.28, P ¼ 0.78). Similarly, there families (Tables IA, B, IIA, B). All of these genera have been was no significant difference in mite diversity between the 2 sites previously recorded from Darwin’s finches (Mironov and Perez, (Fig 2C; D ¼ 3.28, P . 0.10). Since neither prevalence nor 2002; OConnor et al., 2005), with the exception of Analges (found diversity differed significantly between sites, we combined sites on C. olivacea), which has only been recorded from Gala´ pagos within each host species for the analysis of mite abundance vs. mockingbirds (Stefka et al., 2011). host body mass reported below. Before our study, OConnor et al. (2005) used dust-ruffling to quantify feather mites on 24 individuals of a single species of Relation of host body mass to mite abundance Darwin’s finch, G. fuliginosa, from the Santa Cruz lowlands The overall prevalence and abundance of mites collected from (Puerto Ayora). Our lowland (CDRS) results are consistent with each of our 9 Darwin’s finch species are given in Table III. First, OConnor et al. (2005) in that we found the same 5 genera of we compared the abundance of mites among 8 of the 9 finch feather mites. They noted that G. fuliginosa was commonly species (Fig. 3), Camarhynchus psittacula being excluded from the infested (prevalence .25%) with 4 of the 5 genera. The prevalence comparison because of the low sample size (n ¼ 4 sampled of these genera on our birds (Table IB) was similar to those individuals). There was no significant relationship between host reported by OConnor et al. (2005): Proctophyllodes ¼ 29.2% body mass and mite abundance across these 8 host species (n ¼ (Fisher’s exact P ¼ 0.75), Trouessartia ¼ 83.3% (P ¼ 0.44), 760 THE JOURNAL OF PARASITOLOGY, VOL. 99, NO. 5, OCTOBER 2013

TABLE III. Prevalence and abundance (mean 6 SE) of feather mites in Darwin’s finches (OLI [Certhidea olivacea], PAR [Camarhynchus parvulus], FUL [Geospiza fuliginosa], PSI [C. psittacula], SCA [G. scandens], FOR [G. fortis], PAL [Cactospiza pallidus], CRA [Platyspiza crassirostris], MAG [G. magnirostris]). Data for highland (Los Gemelos, LG) and lowland (Charles Darwin Research Station, CDRS) sites are combined.

Feather mite

Host body mass Prevalence Abundance Host (n) (mean 6 SE)* (%) (mean 6 SE)

OLI (20) 9.1 (0.1) 95.0 98.9 (38.0) PAR (29) 12.8 (0.1) 45.0 12.6 (5.8) FUL (41) 13.8 (0.2) 68.3 12.4 (3.6) PSI (4) 18.0 (0.5) 75.0 100.0 (77.1) SCA (21) 21.3 (0.3) 61.9 12.0 (4.1) FOR (39) 21.5 (0.5) 64.1 37.3 (10.9) PAL (12) 22.5 (0.4) 75.0 58.5 (29.4) CRA (23) 31.3 (0.4) 65.2 40.0 (15.0) MAG (10) 32.2 (0.5) 70.0 107.5 (36.2)

* Host body mass in grams.

microclimatic differences between the sites were not of sufficient magnitude to influence the feather mites. For example, Gaede and Knulle¨ (1987) experimentally determined that nonfeeding P. troncatus could not withstand a RH below 55%, causing them to desiccate and die. Since neither highland nor lowland sites reached a RH below 75%, it is unlikely that mite diversity is affected by this abiotic factor. Moreover, if feather mites are affected by microclimatic differences, we can expect that they might shift microhabitats on the body of the host (Wiles et al., 2000) to counteract these effects. It would be interesting to compare the distributions of feather mites on highland and lowland Darwin’s finch species in the future. Unfortunately, the dust-ruffling technique we used did not allow us to compare mite microhabitat distributions. Finally, the lack of difference in mite diversity may be explained by finch dispersal. Galligan et al. (2012) found that during the rainy season when resources are plentiful, G. fuliginosa regularly fly between highland and lowland habitat, resulting in a breakdown of any genetic or ecological barriers that would otherwise separate finch populations. A panmictic population of highland and lowland finches would promote feather mite transmission between host populations and homogenize the mite diversity between the 2 sites. Host body mass is known to have a fundamental influence on the diversity of parasites and other associates (Poulin, 1997; Poulin and Rohde, 1997; Clayton and Walther, 2001; Schmid- Hempel, 2011). We did find a significant relationship between FIGURE 2. Rank abundance plots of feather mite communities from host body mass and feather mite abundance across the 7 of our highlands and lowlands, (A) Geospiza fortis,(B) Geopsiza fuliginosa, and 8 well-sampled (n 10) species of Darwin’s finches. The (C) overall finch assemblages. y-Axes are log transformed. exception to this pattern, C. olivacea, was the only species of finch with significantly more mites than any other species (Fig. Mesalgoides ¼ 45.8% (P ¼ 0.78), and Xolalgoides ¼ 33.3% (P ¼ 3), despite the fact that it is the smallest-bodied species of finch 0.76). sampled. We compared the diversity of Darwin’s finch feather mites at The surprisingly high abundance of feather mites on C. highland and lowland sites on Santa Cruz Island. The 2 sites olivacea may be related to the fact that this species is in severe differed significantly in relative temperature and humidity. decline on Santa Cruz Island. A recent study by Dvorak et al. Despite these differences, we found no significant difference in (2012) estimates that, over the past century, Santa Cruz mite prevalence, abundance, or diversity between the sites. This populations of C. olivacea have declined from more than 1 lack of difference might be explained by the fact that the million males to about 55,000 males, which is a steeper decline VILLA ET AL.—FEATHER MITES ON DARWIN’S FINCHES 761

structure of lice on Western Scrub-jays. Journal of Parasitology 95: 10–13. CLAYTON, D. H. 1991. Coevolution of avian grooming and ectoparasite avoidance. In Bird–parasite interactions: Ecology, evolution and behaviour, J. E. Loye and M. Zuk (eds.). Oxford University Press, Oxford, U.K., p. 258–289. ———, AND D. M. DROWN. 2001. Critical evaluation of five methods for quantifying chewing lice (Insecta: Phthiraptera). Journal of Parasi- tology 87: 1291–1300. ———, J. A. H. KOOP,C.W.HARBISON,B.R.MOYER, AND S. E. BUSH. 2010. How birds combat ectoparasites. Open Ornithology Journal 3: 41–71. ———, AND B. A. WALTHER. 2001. Influence of host ecology and morphology on the diversity of Neotropical bird lice. Oikos 94: 455– 467. DABERT, J., AND S. V. MIRONOV. 1999. Origin and evolution of feather mites (Astigmata). Experimental and Applied Acarology 23: 437–454. DAVIDSON, W. R., D. A. SIEFREN, AND L. H. CREEKMORE. 1994. Seasonal and annual abundance of Amblyomma americanum (Acari: Ixodidae) in Central Georgia. Journal of Medical Entomology 31: 67–71. DUDANIEC, R. Y., B. FESSL, AND S. KLEINDORFER. 2007. Interannual and FIGURE 3. Mean abundance of feather mites (log [n þ 1] 6 SE) for 8 interspecific variation in intensity of the parasitic fly, Philornis downsi, species of Darwin’s finches, arranged in order of increasing body mass: in Darwin’s finches. Biological Conservation 139: 325–332. OLI (Certhidea olivacea), PAR (Camarhynchus parvulus), FUL (Geospiza DVORAK, M., B. FESSL,E.NEMETH,S.KLEINDORFER, AND S. TEBBICH. 2012. fuliginosa), SCA (G. scandens), FOR (G. fortis), PAL (Cactospiza pallidus), Distribution and abundance of Darwin’s finches and other land birds CRA (Platyspiza crassirostris), MAG (G. magnirostris). Different letters on Santa Cruz Island, Gala´ pagos: Evidence for declining popula- indicate significant differences for P , 0.05. See Table III for sample sizes tions. Oryx 46: 78–86. and mean body masses. GAEDE, K., AND W. KNULLE¨ . 1987. Water vapour uptake from the atmosphere and critical equilibrium humidity of a feather mite. Experimental and Applied Acaraology 3: 45–52. than any other species of finch on the island. The authors GALLIGAN, T. H., S. C. DONNELLAN,F.J.SULLOWAY,A.J.FITCH,T. suggest that habitat destruction and herbicides have reduced the BERTOZZI, AND S. KLEINDORFER. 2012. Panmixia supports divergence abundance of insects upon which C. olivacea feeds (Dvorak et with gene flow in Darwin’s small ground finch, Geospiza fuliginosa,on Santa Cruz, Gala´ pagos Islands. Molecular Ecology 21: 2106–2115. al., 2012), implying that birds may devote more time to GALVA´ N, I., E. AGUILERA,F.ATIENZAR´ ,E.BARBA,G.BLANCO,J.L. foraging. A reduction in insects may affect stenotopic species CANTO´ ,V.CORTES´ , O.´ FRIAS´ ,IKOVA´ CS,L.MELENDEZ´ ET AL. 2012. like C. olivacea that are exclusively insectivores much more than Feather mites (Acari: Astigmata) and body condition of their avian eurytopic species that have mixed or seed diets. hosts: A large correlative study. Journal of Avian Biology 43: 273– 279. In addition, invasive parasites may also increase the amount of GAUD, J., AND W. T. ATYEO. 1996. Feather mites of the world (Acarina, time birds need to devote to anti-parasite behavior (O’Connor et Astigmata): The supraspecific taxa (Part I). Annales Musee Royal al., 2010). Since evidence suggests that feather mites are not L’Afrique Centrale Sciences Zoologiques 277: 1–187. parasites, but rather commensals (Galva´ n et al., 2012), mite GRANT, P. R. 1986. Ecology and evolution of Darwin’s finches. Princeton populations may be collaterally influenced by preening (Clayton, University Press, Princeton, New Jersey, 492 p. ———, AND B. R. GRANT. 2008. How and why species multiply: The 1991), which is an important defense against ectoparasites, such radiation of Darwin’s finches. Princeton University Press, Princeton, as feather lice (Clayton et al., 2010). If C. olivacea populations are New Jersey, 218 p. indeed stressed, they may not be able to devote the normal JANOVY, J. 1997. Protozoa, helminthes, and arthropods in birds. In Host– amount of time and energy to preening, which is energetically parasite evolution: General principles and avian models, D. H. Clayton, and J. Moore (eds.). Oxford University Press, Oxford, U. costly (Viblanc et al., 2011). In other words, the abundance of K., p. 303–337. feather mites on Darwin’s finches may be indicative of the poor LINDSTROM¨ , K. M., O. DOLNIK,M.YABSLEY,O.HELLGREN,B.OCONNOR, ‘‘health’’ of the host population. Although this hypothesis is H. PA¨ RN, AND J. FOUFOPOULOS. 2009. Feather mites and internal speculative, it could explain the surprising abundance of feather parasites in small ground finches (Geospiza fuliginosa, Emberizidae) from the Galapagos Islands (Equador). Journal of Parasitology 95: mites on such a small-bodied species of finch. 39–45. ———, J. FOUFOPOULOS,H.PA¨ RN, AND M. WIKELSKI. 2004. Immunolog- ACKNOWLEDGMENTS ical investments reflect parasite abundance in island populations of Darwin’s finches. Proceedings of the Royal Society of London B 271: We thank O. Tiselma and R. Clayton for their help in the field. We 1513–1519. thank the Charles Darwin Research Station for access to historical MAGURRAN, A. E. 2004. Measuring biological diversity. Blackwell weather data records for Santa Cruz Island. The work was supported by Publishing, Oxford, U.K., 256 p. National Science Foundation grant DEB-0816877 to D.H.C., a Natural MALENKE, J. R., N. NEWBOLD, AND D. H. CLAYTON. 2011. Condition- Sciences and Engineering Research Council of Canada Discovery Grant specific competition governs the geographic distribution and diversity to H.C.P., and Sigma Xi Grants-in-aid of Research to J.A.H.K. All of ectoparasites. American Naturalist 177: 522–534. procedures were approved by the University of Utah Institutional Animal MCCLURE, H. E. 1989. Occurrence of feather mites (Proctophyllodidae) Care and Use Committee (protocol #07-08004), and by the Gala´ pagos among birds of Ventura County lowlands, California. Journal of National Park (PC-04-10: #0054411). Field Ornithology 60: 431–450. MERINO, S., AND J. POTTI. 1996. Weather dependent effects of nest LITERATURE CITED ectoparasites on their bird hosts. Ecography 19: 107–113. MIRONOV, S. V., AND T. M. PEREZ. 2002. Two new feather mites (Acari: BUSH, S. E., C. W. HARBISON,D.SLAGER,A.T.PETERSON,R.D.PRICE, Astigmata) from ground finches of the genus Geospiza. Acta AND D. H. CLAYTON. 2009. Geographic variation in the community Parasitologica 47: 228–234. 762 THE JOURNAL OF PARASITOLOGY, VOL. 99, NO. 5, OCTOBER 2013

———, AND H. C. PROCTOR. 2008. The probable association of feather PROCTOR, H. C. 2003. Feather mites (Acari: Astigmata): Ecology, mites of the genus Ingrassia (Analgoidea: Xolalgidae) with the blue behavior, and evolution. Annual Review of Entomology 48: 185–209. penguin Eudyptula minor (Aves: Sphenisciformes) in Australia. RO´ ZSA, L. 1997. Wing-feather mite (Acari: Proctophyllodidae) abundance Journal of Parasitology 94: 1243–1248. correlates with body mass of passerine hosts: A comparative study. ———, AND ———. 2011. Four new species of the family Pteronyssidae Canadian Journal of Zoology 75: 1535–1539. (Astigmata: Analgoidea) from laughing-thrushes (Passeriformes: SCHMID-HEMPEL, P. 2010. Evolutionary parasitology: The integrated study Timaliidae) in China. Acarina 19: 35–51. of infections, immunology, ecology, and genetics. Oxford University MØLLER, A. P. 2010. Host–parasite interactions and vectors in the barn Press, Oxford, U.K., 516 p. swallow in relation to climate change. Global Change Biology 16: STEFKA, J., P. E. A. HOECK,L.F.KELLER, AND V. S. SMITH. 2011. A 1158–1170. hitchhikers guide to the Gala´ pagos: Co-phylogeography of Galapa- gos mockingbirds and their parasites. BMC Evolutionary Biology 11: MOYER, B. R., D. M. DROWN, AND D. H. CLAYTON. 2002. Low humidity 284 doi:10.1186/1471-2148-11-284. reduces ectoparasite pressure: Implications for host life history TOKESHI, M. 1993. Species abundance patterns and community structure. evolution. Oikos 97: 223–228. Advances in Ecological Research 24: 111–186. OCONNOR, B. M., J. FOUFOPOULOS,D.LIPTON, AND K. LINDSTROM¨ . 2005. VIBLANC, V. A., A. MATHIEN,C.SARAUX,V.M.VIERA, AND R. GROSCOLAS. Mites associated with the small ground finch, Geospiza fuliginosa 2011. It costs to be clean and fit: Energetics of comfort behavior in (Passeriformes: Emberizidae), from the Galapagos Islands. Journal of breeding-fasting penguins. PLoS ONE 6: e21110 doi: 10.1371/journal. Parasitology 91: 1304–1313. pone.0021110. O’CONNOR, J. A., J. ROBERTSON, AND S. KLEINDORFER. 2011. Video WALTHER, B. A., AND D. H. CLAYTON. 1997. Dust-ruffling: A simple analysis of host–parasite interactions in nests of Darwin’s finches. method for quantifying ectoparasite loads of live birds. Journal of Oryx 44: 588–594. Field Ornithology 68: 509–518. POULIN, R. 2007. Evolutionary ecology of parasites, 2nd ed. Princeton WILES, P. R., J. CAMERON,J.M.BEHNKE,I.R.HARTLEY,F.S.GILBERT, University Press, Princeton, New Jersey, 332 p. AND P. K. MCGREGOR. 2000. Season and ambient air temperature ———, AND K. ROHDE. 1997. Comparing richness of metazoan influence the distribution of mites (Proctophyllodes stylifer) across the ectoparasite communities of marine fishes: Controlling for host wings of blue tits (Parus caeruleus). Canadian Journal of Zoology 78: phylogeny. Oecologia 110: 278–283. 1397–1407.